(Stroke. 1995;26:1543-1547.)
© 1995 American Heart Association, Inc.
Articles |
Asymmetrical Skin Temperature in Ischemic Stroke
From the Department of Neurology, University of Oulu (J.T.K., K.A.S., V.V.M.); and the Department of Neurological Rehabilitation, Deaconess Institute of Oulu (J.T.K.), Oulu, Finland.
Correspondence to Dr Juha Korpelainen, Department of Neurology, University of Oulu, Kajaanintie 50 A, FIN-90220 Oulu, Finland.
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Abstract |
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Background and Purpose Sympathetic dysfunction is known to manifest commonly in stroke as cardiovascular and sudomotor dysregulation, but the knowledge so far obtained concerning skin temperature and vasomotor changes in cerebrovascular diseases is contradictory. The purpose of the present study was to evaluate cutaneous temperature in ischemic stroke in a prospective follow-up study.
Methods Skin temperature was measured at five sites on each side of the body at rest and after a heating stimulus in 44 patients with a hemispheric infarction, and in 19 patients with a brain stem infarction, in the acute phase and at 1 month and at 6 months after the infarction.
Results Skin temperatures on the forearm, leg, and foot on the side contralateral to the site of infarction were significantly lower than on the ipsilateral side during the whole 6-month follow-up period. Asymmetrical temperature was associated with the presence of pyramidal tract signs in hemispheric infarction and with the presence of Wallenberg's syndrome in brain stem infarction. In hemispheric infarction, the degree of asymmetrical temperature correlated with the severity of limb paresis.
Conclusions A temperature decline in the limbs contralateral to the site of infarction seems to be a frequent, long-lasting consequence of autonomic failure in patients with stroke. The phenomenon seems to be associated with pyramidal tract signs and the presence of Wallenberg's syndrome.
Key Words: autonomic dysfunction • cerebral infarction • temperature • vasomotor system
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Introduction |
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Cerebrovascular diseases are known to include features of autonomic dysfunction in their symptomatology, with the most common disorders being cardiovascular1 and thermoregulatory complications.2 3 4 Hyperhidrosis on the paretic side of the body, reflecting central sympathetic dysregulation, is frequently seen in patients with a hemispheric brain infarction.2 4 Moreover, brain stem infarction often results in hypohidrosis on the side ipsilateral to the infarction.3 In addition to abnormal sweating, some patients with stroke also complain of coldness on the paretic side of the body and in the paretic limbs.
Asymmetrical skin temperatures reflecting vasomotor autonomic dysregulation have been described in stroke patients,5 6 7 8 9 10 11 12 but the results of these previous studies are contradictory, with some studies reporting increased5 7 9 and others decreased10 11 12 skin temperatures in the paretic limbs. Moreover, Wanklyn et al12 recently reported lower finger skin temperatures and reduced blood flow to the paretic hand at rest and after cold stress in 10 patients with symptoms of coldness in the hand. However, those previous studies were carried out on small patient populations and without modern quantitative measurement and imaging technology, and no prospective investigations were made.
In the present prospective 6-month follow-up study, skin temperatures were measured in patients with ischemic stroke at rest and after heating provocation bilaterally at five registration sites: forehead, chest, forearm, leg, and foot. The aim was to evaluate the prevalence, degree, and clinical characteristics of temperature regulation associated with hemispheric and brain stem infarctions.
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Subjects and Methods |
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The study was carried out in the Department of Neurology, Oulu University Hospital, with the approval of the ethics committee of the medical faculty, University of Oulu. All patients gave informed consent to participate in the study.
Sixty-three consecutive patients (42 men and 21 women; mean±SD age, 54.3±10.8 years; range, 19 to 69 years) with acute brain infarction were included in the study. Patients with manifestations of other central or peripheral nervous system lesions and patients with any other disease (eg, diabetes mellitus or alcoholism) known to affect the autonomic nervous system were excluded. In 44 patients, the infarct was located at the hemispheric level (20 in the right and 24 in the left hemisphere) and in 19 patients at the brain stem level (11 medullary and 8 pontine).
Forty-two of the 44 patients with a hemispheric infarction had unilateral signs of pyramidal tract lesion; most of them also had sensory deficits, while 2 patients had only aphasia. Eight of the 19 patients with a brain stem infarct had the lateral medullary syndrome of Wallenberg: Horner's syndrome, limb ataxia, pharyngeal weakness and facial sensory deficits on the side ipsilateral to the infarction, and sensory deficits of the body and the limbs on the side contralateral to the infarction. Three further patients with medullary infarction had ipsilateral Horner's syndrome, bulbar paresis, and contralateral sensory deficits of the body and the limbs. Eight patients had a pontine infarction resulting in either contralateral hemiparesis or impaired pain and thermal sensation associated with bulbar paresis, external ophthalmoplegia, or ipsilateral facial sensory deficit.
Cerebral CT was performed on all the patients on admission to the hospital and was repeated within 2 weeks if the first examination was negative. A hemispheric infarction was verified by CT in 40 cases; brain stem infarction was verified in 3 cases. Even the repeated CT examination with contrast remained normal in 4 patients with clinical signs of a hemispheric infarction and in 16 patients with signs of a brain stem infarction.
Forty-four of the 63 patients had no preexisting disease or medication known to affect the autonomic nervous system. Twelve patients had arterial hypertension, 6 had coronary heart disease, and 5 had long-term atrial fibrillation. Nineteen patients were taking cardiovascular medication: 9 digitalis medication, 8 ß-adrenergic blocking agents, 8 diuretics, 7 calcium entry blockers, 2 angiotensin-converting enzyme inhibitors, and 1 nitroglycerin.
All the patients were examined by one of the authors (J.T.K.) in the acute phase and at 1 month and 6 months after the infarction, with special attention being given to the neurological deficits caused by the brain infarction and to the symptoms and signs suggestive of autonomic dysfunction. Before the examination, all the patients were asked about the presence of a feeling of cold on either side of the body. For quantifying the degree of muscle weakness, the following rating scale was used: 0, complete paralysis; 1, minimal contraction; 2, active movement with gravity eliminated; 3, weak contraction against gravity; 4, active movement against gravity and resistance; and 5, normal strength.
Skin surface temperatures were recorded with a digital thermometer (TC-1100, Line Seiki) between 1 and 7 days after the infarction (median, 4 days), and the measurements were repeated 1 month and 6 months later. Fifty-eight patients were available at the time of the 1-month visit and 52 at the 6-month follow-up visit.
The investigations were performed by a single examiner (J.T.K.) in the same experiment room at a standard temperature of 24.0±0.5°C; the mean relative humidity of the room was kept at approximately 47%, and all draft was eliminated. Before the experiment, the patients were allowed to acclimatize to the temperature of the room for 30 minutes. Skin temperatures were recorded at a baseline and after 10 minutes of heating bilaterally at five registration sites: forehead, chest, forearm, leg, and foot. The heating stimulus was provided by four standard thermal packings (75°C, 1000 W) placed on the abdomen. In addition, the reclining subject was covered with a non–heat-penetrating blanket from the upper chest to the knees to prevent heat escape. The same method has previously been used in studying sweating dysfunction in brain infarction.2 3 4
The statistical analyses were performed with the Wilcoxon matched-pairs test comparing the temperatures on the ipsilateral and contralateral sides of the body. Linear regression analysis was used for correlating muscle weakness with the difference in temperature between the ipsilateral and the contralateral sides. The significance level for the asymmetry in temperature between the clinical subgroups of infarct patients was assessed with the Mann-Whitney two-sample test.
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Results |
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Thirty-eight (60%) of the 63 patients reported a subjective feeling of cold on the side of the body contralateral to the infarction when compared with the ipsilateral side during the 6-month follow-up period. Twenty-six (60%) of the 44 patients with a hemispheric infarction and 12 (63%) of the 19 patients with a brain stem infarction had recognized the phenomenon. None of the patients complained of coldness on the ipsilateral side.
The mean differences of the skin temperatures at the five registration
sites between the sides contralateral and ipsilateral to the infarction
are presented in Table 1
. The mean temperatures
on the side contralateral to the infarction were significantly lower
than those on the ipsilateral side on the forearm, leg, and foot. A
significant difference was seen in both limbs during the whole 6-month
follow-up period and also on the chest in the acute phase. A similar
asymmetry in temperatures was also found after the heating
stimulus.
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Tables 2 and 3 present the mean skin
temperatures at the five registration sites on both sides of the body
at baseline and after the heating stimulus in patients with hemispheric
brain infarction. The mean temperatures on the side contralateral to
the infarction were significantly lower than those on the ipsilateral
side on the forearm, leg, and foot during the whole 6-month follow-up
period. In the acute phase and at 6 months, a significant difference
was also found on the chest.
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The patients with a hemispheric brain infarction showed a linear
correlation between muscle weakness and the temperature difference. A
significant correlation was found in the acute phase in the leg
(P=.001, r=.519), at 1 month in the leg
(P=.0001, r=.758), and in the foot
(P=.0003, r=.671) and at 6 months in the forearm
(P=.001, r=.625), in the leg (P=.0004,
r=.664), and in the foot (P=.003,
r=.585). The skin temperatures were only asymmetrical in the
hemispheric infarct patients with spasticity, accelerated tendon
reflexes, extensor plantar response, and facial paresis (Table 4). The presence of asymmetry was not related to the
side of the infarct or the presence of sensory deficits. Two patients
were left-handed and all the others were right-handed. The results of
these two patients did not differ significantly from the results of the
others.
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In the group of patients with a brain stem infarction, the temperatures
on the side contralateral to the infarction were lower than those on
the ipsilateral side only in the patients with medullary infarction
(Tables 5 and 6). At baseline, a
significant difference was seen in the acute phase on the leg and the
foot and at 1 month on the leg, but no difference was observed at 6
months after the infarction. After the heating stimulus, the
temperature difference was significant on both limbs in the acute
phase. All of these patients had Horner's syndrome, reflecting a
deficit of the sympathetic nervous system.
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The results of the patients with pontine infarction are
presented in Tables 7 and 8. In
these patients, the temperature differences were not significant.
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Discussion |
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There are only a few previous investigations focusing on the altered skin temperature in patients with cerebral lesions. Most of these studies5 6 7 8 were carried out years ago without modern imaging and other measurement technology, and that may explain the contradictory results. More sensitive thermometric and thermographic methods have shown the paretic upper limb to be colder than the unaffected limb.10 11 12 The coldness of the paretic side is mainly related to skin vasomotor changes. In a recent plethysmographic study12 of 20 hemiplegic patients, blood flow to the paretic hand was reported to be significantly reduced at rest and after cold stress in patients who feel coldness in the paretic hand, but the lower limbs were not studied.
In the present prospective series, we demonstrated a significant asymmetry in skin temperatures in patients with brain infarction, with the limbs contralateral to the infarction being markedly colder than the ipsilateral ones. A majority of the patients had recognized the phenomenon themselves. Sixty percent of the patients with hemispheric infarction and 63% of the patients with brain stem infarction reported a subjective feeling of coldness in the limbs contralateral to the infarction. The coldness was often recognized as early as the acute phase, but more commonly it was identified later on during the follow-up, although the temperature asymmetry was more marked in the acute phase. It seems that the symptoms do not manifest themselves until the subject becomes exposed to cold or heat in his or her "normal life." The phenomenon could be demonstrated by a thermometer, but it was also commonly observed clinically.
In previous studies,10 11 12 the feeling of coldness typically was reported as involving the paretic hand and arm. However, the present study revealed a significant asymmetry of temperatures in both the upper and lower limbs and in the acute phase in the chest as well. The most marked differences of temperature were found in the leg and the foot, where the maximum value of the difference reached 6.8°C. In many cases, the affected limb was 4°C to 6°C colder than the unaffected one. These patients were well aware of this unpleasant symptom, which significantly impaired their quality of life and especially limited their outdoor activities during cold weather.
The results of the present study suggest that in hemispheric brain infarction the coldness of the paretic limbs is associated with clinical signs of the pyramidal tract lesion. The coldness was more pronounced in the patients with severe paresis, spasticity, accelerated tendon reflexes, extensor plantar response, and facial paresis than in the patients without these signs. The presence of sensory deficits, the side of the infarct, and the brain dominance were not related to the phenomenon. Thus, it seems that the coldness of the paretic limbs is associated with the severity of the clinical manifestations of the patient rather than with the location of the infarction.
In patients with brain stem infarction, asymmetrical skin temperature was linked to the presence of Horner's syndrome, reflecting a unilateral deficit of the sympathetic nervous system. Most of these patients had the lateral medullary Wallenberg's syndrome, but none of them had hemiparesis or any other signs of a pyramidal tract lesion. In patients with pontine infarction, no significant asymmetry of the skin temperatures of the limbs could be detected, although 6 of the patients had pyramidal tract signs. The finding may be related to the small number of the patients.
Local skin temperature is regulated by two sympathetic effector organs, cutaneous blood vessels and sweat glands, under the control of the central nervous system.13 14 The activity of these organs is affected by thermal and mental stimuli. Body cooling leads to an increased outflow of cutaneous vasoconstrictor impulses, and respectively, body heating decreases the number of vasoconstrictor impulses and increases the number of sudomotor impulses. The increase of blood flow through the forearm, as well as upper arm, thigh, and calf, is elicited largely by active vasodilatation and only to a small degree by decrease of vasoconstrictor activity, but the increase of blood flow through the hands and feet is elicited by a decrease of vasoconstrictor activity.14 15 Moreover, an emotional stimulus may cause a simultaneous activation of vasoconstrictor and sudomotor fibers, constituting the basis for a "cold sweat."13 14 The most important thermoregulatory center of the central nervous system is the hypothalamus, which receives information from cutaneous and internal thermoreceptors. The efferent vasomotor and sudomotor pathways originate in the hypothalamus, descend mainly uncrossed to the mesencephalon, pons, and posterolateral medulla oblongata, and transmit to the preganglionic neurons in the intermediolateral column of the thoracolumbar spinal cord. Preganglionic neurons synapse in the paravertebral ganglia with the postganglionic neurons that innervate cutaneous blood vessels and sweat glands.14 16 The cerebral cortex has contralaterally distributed facilitatory and inhibitory effects on vasomotor and sudomotor activity, which are involved in emotional rather than thermoregulatory activity.14 16 17
The observed coldness of the paretic limbs could be explained by a decrease of the cortical or subcortical inhibitory effect on the vasomotor neurons, resulting in increased vasoconstrictor tone with decreased cutaneous blood flow and skin temperature in the side opposite to the infarction. The phenomenon may be modulated by simultaneous changes in vasodilatation activity. Similarly, a release of the cortical sympathoinhibitory input to the sudomotor neurons has previously been shown to cause hyperhidrosis throughout the paretic side of the body in patients with a hemispheric brain infarction.2 4 18 19 Further evidence for this suggestion may be derived from experimental14 and human microneurographic13 studies of central and peripheral neural lesions. In patients with spinal cord injury, sympathetic vasomotor activity below the lesion is increased because of reduced supraspinal inhibition to sympathetic vasomotor neurons.13 20 21 Muscle vasomotor activity has also been shown to be increased in patients with Guillain-Barré syndrome,22 which may be associated with a reduced inhibition of brain stem vasomotor centers.
In our patients with medullary brain infarction, the observed asymmetry of cutaneous temperatures is probably caused by damage in the medullary vasomotor centers. It is well known that in patients with Horner's syndrome the ipsilateral side of the face is warmer and hypohidrotic compared with the other side. In our series, the ipsilateral side of the face was warmer than the contralateral side in 6 patients, and colder in 3; 2 patients had symmetrical facial temperature. It seems that in some cases Horner's syndrome may be partial, manifesting as ipsilateral myosis, ptosis, and hypohidrosis with normal facial temperature.
Other mechanisms may also cause reduced blood flow and decreased cutaneous temperature on the paretic side of the body. Simple disuse of the paretic limb could affect the vasomotor tone of the proximal parts of the limbs with large muscle groups but not the hands and feet with proportionately more skin and less muscle, as suggested by Wanklyn et al.12 Moreover, none of our patients had pain or other symptoms of reflex sympathetic dystrophy that might also be related to asymmetrical temperature.23 Furthermore, cutaneous vasoconstriction may be associated with humoral or local endogenous vasoconstrictive agents.
In conclusion, brain infarction seems to cause a significant asymmetry of skin temperatures, with the limbs contralateral to the infarction being markedly colder than the ipsilateral ones in a majority of patients. The phenomenon is associated with pyramidal tract signs in hemispheric infarction and with the presence of the lateral medullary Wallenberg's syndrome in brain stem infarction.
Received January 24, 1995; revision received March 20, 1995; accepted June 23, 1995.
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